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Auxin Transport – Shaping the Plant

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Auxin Transport – Shaping the Plant 7 Auxin transport Ð shaping the plant JirÏõÂ Friml Plant growth is marked by its adaptability to continuous changes answer to their sessile fate and which became their major in environment. A regulated, differential distribution of auxin adaptation strategy. Special meristem tissues have underlies many adaptation processes including organogenesis, evolved, which maintain the ability of plant cells to divide meristem patterning and tropisms. In executing its multiple roles, and differentiate throughout the life of the plant, and a auxin displays some characteristics of both a hormone and a number of differentiated cells keep their potential to morphogen. Studies on auxin transport, as well as tracing the elongate, forming the basis of plant tropisms. Thus, plants intracellular movement of its molecular components, have can ¯exibly change their shape and size to optimally suggested a possible scenario to explain how growth plasticity is adjust themselves to a changing environment. During conferred at the cellular and molecular level. The plant perceives the past century, an endogenous plant signal, auxin, and stimuli and changes the subcellular position of auxin-transport its distribution in the plant have been increasingly estab- components accordingly. These changes modulate auxin ¯uxes, lished as playing a central role in these complex adapta- and the newly established auxin distribution triggers the tion responses. Recently emerging molecular data have corresponding developmental response. shed light on the mode of auxin action and its regulated transport, and have begun to connect the plasticity of Addresses whole-plant development with processes at the cellular Zentrum fuÈ r Molekularbiologie der P¯anzen, UniversitaÈ tTuÈ bingen, Auf level. der Morgenstelle 3, 72076 TuÈ bingen, Germany e-mail: [email protected] A century towards molecular players Our linden tree had to wait more than 300 years before our Current Opinion in Plant Biology 2003, 6:7±12 curiosity was turned towards the mysterious mechanisms that so strangely affected its fate. At that time, a German 1369-5266/03/$ ± see front matter botanist, Julius Sachs, proposed the existence of signaling ß 2003 Elsevier Science Ltd. All rights reserved. substances that regulate coordinated plant growth, and DOI 10.1016/S1369-5266(02)00003-1 Charles Darwin together with his brother Francis grew grass coleoptiles in unilateral light to demonstrate the Abbreviations existence of a transported signal that mediates plant AUX1 AUXIN1 phototropism [1,2]. Thus, the history of auxin began. IAA indole-3-acetic acid During the century that followed, the chemical nature MDR multidrug resistance of auxin was uncovered, but we remained confused by the PIN PIN-FORMED SGR2 SHOOT GRAVITROPIC2 variety of apparently unrelated developmental processes ZIG ZIGZAG that are regulated by such a simple molecule as indole-3- acetic acid (IAA). Prelude Ð The linden tree of innocence Our attention was drawn to the transport of auxin, as its On the margin of the ChirÏiby hills, an old mediaeval castle disruption interferes with almost all auxin-related devel- `Buchlov' guards the wide valley of the South Moravian river opmental processes. We learned that auxin can be dis- `Morava'. There, on the terrace where the tribunal of the hunter's tributed via the phloem or by a directional, so-called court used to sit, and where the last farewells with the convicts `polar', transport system (see Figure 1; [3]). The large were held, a famous linden tree of innocence stands as a witness amount of physiological and biochemical data on polar of a local legend. It is told that early in the 16th century the lord auxin transport has been integrated into the `chemiosmo- of the castle was deceitfully slain during one of his frequent hunts. tic hypothesis'. This classical model explains the cell-to- A young servant was accused of this murder and imprisoned. cell movement of auxin by the action of speci®c auxin- After long days of unavailing torture he was condemned to death in¯ux and -ef¯ux carriers. The asymmetric positioning of on the castle terrace. At this, the young man rose and pulled out the latter at a particular side of the cell was proposed to the young linden tree growing nearby. He set it inverted back into determine the direction of auxin ¯ux [4,5]. This model the soil with the words, ``If next year this small tree will grow was reinforced by the identi®cation and characterization green, it will be a sign of God that you killed an innocent''. And of candidate proteins for auxin in¯ux (AUXIN1 [AUX1]/ indeed, in the spring, small green leaves ¯ourished from the LIKE-AUX1 [LAX] family) and ef¯ux (PIN-FORMED previous roots and the young man was set free. [PIN] family) carriers [6±8]. Numerous pieces of circum- stantial evidence demonstrate the role of these proteins in This rather romantic story demonstrates the fascinating auxin transport despite the lack of rigorous proof for their plasticity of plant growth, which plants developed as an function as carriers [3]. PIN proteins are asymmetrically www.current-opinion.com Current Opinion in Plant Biology 2003, 6:7±12 8 Growth and development Figure 1 lamic acid (NPA), an inhibitor of auxin transport, thus providing an additional connection between MDRs and auxin delivery [14]. Although detailed information is still lacking, a century of studies on auxin transport have brought us the identity of a couple of players that are involved in auxin responses, and an image of a complex network of several transport systems that are involved in distributing auxin throughout the whole plant. Hormone or morphogen? Two theoretical concepts have greatly in¯uenced the way that we think about auxin and its action: the concepts of a hormones and a morphogen. The mammalian hormone concept de®nes hormones as extracellular signaling mole- cules, which act on target cells distant from their localized site of synthesis [15]. Although recent studies have demonstrated the potential for IAA synthesis in a variety of Arabidopsis organs, its movement from its main source in young apical tissues throughout the whole plant has been proven many times [3,16]. A known role for auxin in coordinating the development of organs, for example lateral roots, with the developmental stage of the shoot provides a functional meaning for this long-distance sig- naling [17,18]. Thus, auxin formally adheres to the clas- Gravity sical de®nition of a hormone. However, the most-studied form of auxin transport, cell-to-cell polar transport, con- trasts with the passive allocation of animal hormones through blood, which is more analogous to non-polar auxin distribution. Several arguments indicate that Current Opinion in Plant Biology non-polar transport in phloem contributes to the move- ment of auxin from its main source in the apical tissues to Auxin response and transport in a gravistimulated Arabidopsis hypocotyl. Auxin transport throughout the plant involves both non-polar the root. First, the known velocity of active transport transport in phloem (dashed line) and an active, cell-to-cell polar (about 10 mm per hour) is too slow to execute ef®cient transport (red arrows), which can transport auxin either basipetally signaling, especially in larger plant species. Second, free (from the apexto the base) or laterally. During gravitropic or phototropic auxin has been detected at relatively high concentrations bending, increased auxin response (as indicated by DR5::GUS, displayed as blue staining) corresponding to higher auxin levels is found (of about 1 mM) in phloem exudates [19]. And third, aux1 in the more elongated, outer side of bending hypocotyl. This mutants, which are apparently impaired in loading auxin asymmetric lateral auxin distribution appears to be established by from leaves into the phloem and in unloading auxin from lateral auxin transport and to trigger asymmetric growth. phloem into the root, display defects in their ability to distribute auxin between the shoot apex and the root [12,20]. Thus, the putative auxin permease AUX1 localized in different cells, and this localization impres- seems to act at both ends of the auxin route in phloem, sively coincides with the known directions of auxin ¯ux connecting it at its lower end to the polar transport system [8,9,10,11]. The AUX1 protein also localizes asymme- in the root tip. trically in root protophloem cells at the opposite cell side from PIN1 [12]. These ®ndings suggest that, at least in In the root meristem, auxin is implicated in regulating the some tissues, in¯ux and ef¯ux carriers in concert facilitate pattern of cell division and differentiation (see Figure 2), the vectorial movement of auxin. Recently, members of a short-distance activity that is related to the role of auxin another protein family, namely multidrug resistance as morphogen. The term morphogen was introduced as a (MDR)-type ATP-binding cassette (ABC) proteins, have purely theoretical term in mathematical models of self- been implicated in auxin transport. Two of these proteins, organizing systems, and has evolved into a basic concept AtMDR1 and Arabidopsis thaliana P-glycoprotein1 of developmental biology [21]. The least stringent de®ni- (AtPGP1), were originally identi®ed as being functionally tion refers to a morphogen as a substance that forms a related to anion channels; nonetheless, the corresponding concentration gradient and is involved in developmental mutants and double mutants showed auxin-related phe- patterning [21]. More rigorous de®nitions provide three notypes including a reduced rate of auxin transport [13]. critical conditions that bona ®de morphogens must meet: Moreover, these proteins can bind 1-N-naphthylphtha- ®rst, a morphogen forms a stable concentration gradient; Current Opinion in Plant Biology 2003, 6:7±12 www.current-opinion.com Auxin transport Friml 9 Figure 2 How does the auxin gradient arise? In the root, the auxin ef¯ux regulator PIN4 is asymmetrically distributed towards cells with increased DR5 response, and both Epi pin4 mutations and the chemical inhibition of auxin Cor Ste transport disrupt the distribution of DR5 activity End [11,26].
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